Serotonin and Dominance
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KeywordsSelective Serotonin Reuptake Inhibitor Serotonin Transporter Dominance Hierarchy Social Hierarchy Short Allele
Dominance describes high status of an individual in social hierarchy that allows for priority access to limited resources such as food, mates, and space. Serotonin, a monoamine neurotransmitter, contributes to the formation of social hierarchy and positively affects dominance in humans and other primates.
Social hierarchy is a key element in the organization of many human and nonhuman groups that undertake collective and cooperative activities. Dominant group members standing at the top of the hierarchy are privileged with various benefits including priority access to limited resources (food, mates, space) over the subordinate members. In order to maintain their position, dominant individuals exercise behavioral tactics that rely on subtle interplay between cooperation, affiliation, and aggression directed toward subordinates. In contrast, submission, although limits the access to resources, allows weaker and less skillful individuals to minimize consequences of aggressive encounters with conspecifics.
Misinterpretation or ignorance of the social dominance structure has profound consequences for individual’s life including aggression from conspecifics, exclusion from the social group, or death (Watanabe and Yamamoto 2015). Because of this, one can expect that during evolution, there had to be a selection pressure on efficient neurophysiological mechanisms for recognizing and interpreting cues for social status in conspecifics and expressing social status of oneself. Neuroscientific studies conducted during the last decade helped to elucidate these mechanism and pointed to the important role of serotoninergic system in establishing of the social hierarchy both in primates and in humans (Kiser et al. 2012).
Serotonin and Social Hierarchy
Serotonin (5-HT) is a conservative monoamine neurotransmitter derived from the amino acid l-tryptophan, found in all bilateral animals. In the central nervous system (CNS), primary sources of 5-HT production are raphe nuclei located in the brainstem; however, 90 % of serotonin is synthesized outside CNS, in gastrointestinal tracts. The synthesis of serotonin in the brain is dependent on the availability of its precursor amino acid, tryptophan. Serotonin is reabsorbed from synapses through serotonin transporter located on the presynaptic neuron, and levels of synaptic serotonin might be regulated via selective serotonin reuptake inhibitors (SSRI). Degradation of 5-HT in the brain is mediated by monoamine oxidase A (MAOA), which results in producing 5-hydroxyindoleacetic acid (5-HIAA).
Serotonin was found to directly support dominance structure in primate groups. Studies conducted in vervet monkeys (Cercopithecus aethiops) demonstrated that alpha-male individuals had higher levels of blood and brain serotonin that decreased when dominant position was lost (Raleigh 1984). Furthermore, experimentally induced rise in 5-HT level promoted dominance acquisition in these animals (Raleigh et al. 1991). Similar effects were observed in humans. Experimental treatments with tryptophan and selective serotonin reuptake inhibitor (both act to rise 5-HT level) were associated with increased self-assessed dominance (Moskowitz et al. 2003), increased dominance judgments by peers, and dominant pattern in a stranger-dyadic social interaction (Tse and Bond 2002) in healthy men and women.
Studies in several different areas such as serotonin involvement in processing of facial cues, voice cues and mechanisms of aggression and cooperation elucidates how serotoninergic system affects recognition and the establishment of social dominance structure.
Serotonin Affects Facial Cues Recognition
Social status is most frequently signaled in close proximity. In such conditions, individual’s face represents an ideal source of transmission of the dominance signals and facial expression constitutes one of the best recognizable cues to communicate social status. Numerous studies confirmed that people, similarly to primates, read and identify cues of dominance from various characteristics of the face such as shape, facial expression, or gestures (Keating 1985; Little et al. 2007; Re et al. 2013). It is hypothesized that these facial clues evolved from the preparatory or support responses associated with attack or defense. Facial characteristics such as chin prominence, heaviness of brow ridges, and facial muscularity were also found to be predictive on current and future social status and reproductive success of their holders (Mueller and Mazur 1997; Rule and Ambady 2010).
Facial expression perception depends on serotoninergic system, and 5-HT level influences recognition of emotion from the face (Harmer 2008). Higher synaptic 5-HT level induced by repeated administration of selective serotonin reuptake inhibitors (SSRI) is associated with decreased accuracy of recognizing angry, fearful, and disgusted faces (Harmer et al. 2003) and increased tendency to interpret ambiguous faces as happy (Harmer et al. 2004). In addition, the same experimental procedure is associated with reduced neurophysiological response to fearful faces from the amygdala, hippocampus, and medial prefrontal cortex observed in functional magnetic resonance imaging (FMRI) (Harmer et al. 2006). These observations suggest that dominant individuals characterized by higher 5-HT levels (Raleigh 1984) might be less responsive to angry and fearful faces and react with lower anxiety to threats from conspecifics. In contrast, submissive individuals with lower 5-HT levels might be more sensitive to angry expressions, which allow them to avoid aggressive attacks from dominants.
Serotonin Affects Voice Processing
Voice is another important cue to social status. Voice pitch in male primates, including humans, is associated with testosterone level (Dabbs and Mallinger 1999) and perceived attractiveness and dominance (Puts et al. 2006), thus might be indicative of reproductive success. Moreover, studies on CEO’s of companies registered on the American Stock Exchange showed that voice may also predict professional status and income – CEO’s with lower voices make more money and enjoy longer tenures at the companies (Mayew et al. 2013). Interestingly, polymorphism in serotonin transporter gene (5-HTTLPR), which regulates synaptic serotonin concentrations and possibly modulates dominance hierarchy (Miller-Butterworth et al. 2007), is also associated with voice perception and processing. In particular, study finds that carriers of the short allele of 5-HTTLPR, associated with increased synaptic serotonin level, showed a decreased differentiation in the event-related potential (ERP) responses elicited by happy and angry tone of voice. The number of short alleles was associated with linear decrease in the amplitude of the ERP in response to a happy voice. This suggests that the facilitatory effects of processing positive (happy) voices were reduced in individuals carrying the short allele. In contrast, facilitation through positive voices was strongest for individuals homozygous for the long allele (Grossmann et al. 2013).
Serotonin Affects Aggression, Cooperation, and Affiliation
To reach and maintain dominant rank in social hierarchy, individuals use specific tactics that include mixture of affiliative, cooperative, and aggressive behavior. The intensity of each of these behaviors depends on species, its social organization, and ecological niche. While general aggressiveness and physical strength defines position of the individual in the social hierarchy of simply organized groups, these characteristics are insufficient in communities where cooperative skills are required (Kiser et al. 2012).
Serotoninergic system was demonstrated to support all of these behaviors, i.e., aggression, cooperation, and affiliation, however not in a simple manner. In vervet monkeys, subordinate group members treated with serotonin enhancers achieved dominance by first increasing affiliative behavior toward group members and creating support group. During this period, aggressive behavior significantly decreased, while affiliative behavior (approaching and grooming) was significantly increased. Only after coalitions with other individuals were established dominant individuals engaged in aggressive encounters with conspecifics (Raleigh et al. 1991). Similar effect was observed in humans – application of selective serotonin reuptake inhibitor to the subjects was associated with increase in peer-rated dominance and increased eye contact when subjects were speaking. At the same time, subjects were more prone to reduce their award in favor of their opponents and increase number of cooperative messages sent to opponents during the mixed-motive games (Tse and Bond 2002). These observations concur with general effects of serotonin on aggression and cooperation. Experimental studies conducted in humans and nonhuman primates confirm that serotonin depletion increases aggression (Siever 2008), learning of cooperation, and perception of trustworthiness (Wood et al. 2006).
Neurophysiological studies conducted in nonhuman primates and in humans suggest an important role of serotoninergic system in shaping dominance hierarchy. Results of these studies demonstrate serotonin involvement in mechanism of achieving and maintaining dominant rank in social hierarchy. They also highlight possible alterations in dominant and submissive processing of emotions from nonverbal characteristics, such as face expression and voice pitch that signal social status. These alterations might result from differences in serotoninergic system activity between dominant and submissive individuals.
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